The effect of prior leaning on human postural responses

Gait & Posture 1993; 1: 203-210

The effect of prior leaning human postural responses

F B Horak, S P Moore

on

RS Dow Neurological Sciences Institute, Good Samaritan Hospital and Medical Center, Portland, OR, USA

Summary

This study examines how human postural responses are altered by leaning about the ankles to five different initial stance positions prior to anterior or posterior horizontal translations of the support surface. When subjects leaned in the same direction as the translation-induced sway, postural strategies changed to use of less ankle torque and more horizontal shear forces at the surface to return to equilibrium. This change in strategy was associated with reduced and delayed activation of the stretched ankle muscles and an increased activation of proximal muscles producing rapid hip flexions or extensions. The changes in ankle muscle activation strength and latencies cannot be predicted based on simple stretch or load reflexes, but match predictions from computational, biomechanical models of human stance co-ordinationla.

Key words: Posture, EMG, model, stretch reflex, electromyography

Introduction

There is considerable evidence that the co-ordination of automatic postural responses to unexpected perturbations of stance changes depending upon the functional, biomechanical demands of the taskslo. Although it is generally accepted that stereotyped reflex models cannot account for the robust flexibility of even the shor- test latency postural responses, the neural mechanisms for these functional changes are not well understood”. The functional flexibility of postural responses has been attributed to adaptation, habituation, summation, gaiting, or switching of local reflexes based on well- established laws for modification of proprioceptive reflexes by peripheral conditions such as muscle length, load, preactivation, etc.12m’6. It is generally accepted that the CNS can modify the gain of even simple reflexes based on expectation, instruction and experience17m19. More complex central sculpting of triggered co-ordinative programs based on internal representations of body and environmental constraints have also been suggested

Received: 25 January 1993 Accepted: 17 September 1993 Correspondence und reprint requests to: Fay B Horak PhD, RS Dow Neurological Sciences Institute, 1120 NW 20th Avenue, Portland, OR 97209, USA

@I 1993 Butterworth-Heinemann Ltd 096&6362/93/04203-08

but whether these programs are selected discretely from a limited repertoire or vary continuously depending on the infinite biomechanical demands remains contro- ~ersialll.?O-?5.

A good example of the functional flexibility of postural responses not easily explained by modification of local reflexes is the gradual change from ankle to hip sway when subjects stand across a narrow surfacez6. When ankle torque of standing subjects is limited by standing across a surface shorter than the length of their feet, subjects alter their postural movement strategy from an inverted pendulum sway about the ankles associated with early ankle muscle activation and large torques at the surface called the ‘ankle strategy’ to a 3:1 combination of hip to ankle angle sway associated with early hip and reduced ankle muscle activation and additional horizontal shear force at the surface called the ‘hip strategy’26. It requires several trials responding to perturbations after a change in support surface for subjects to arrive at a new, stable co-ordinative pattern but the short response latencies never vary suggesting that the new, efficient strategy is learned iteratively and triggered as a preprogrammed unit based on prior experience”. Nashner and McCollum’ established a theoretical basis for analysing postural co-ordination in which they suggested that the CNS preselects a discrete postural strategy from a limited number of preprogrammed synergies in order to return to equilibrium. This theoretical model predicts selection of proximal muscles to flex or extend

204 Gair & Posture 1993; 1: No 4

the hips to move body centre of mass whenever the ability of ankle muscles to exert torque on the surface is limited.

A new computational optimal control model of human stance co-ordination predicts a gradual, rather than a discrete, change from ankle to hip strategy depending upon how fast the centre of body mass must be accelerated to maintain equilibrium2v3. This model has unified the ankle and hip strategies into a single set of dynamic criteria in which primarily ankle acceleration is employed to the extent that toe- and heel-off constraints allow, and further acceleration of the centre of body mass is then achieved by a combination of hip and ankle accelerations which result in increased surface reactive shear forces. A similar change from ankle to more hip strategy should occur whether the support surface becomes narrow or the body gets near the boundary of stable posture by leaning, since hip motions and muscle activations would be added to ankle whenever very rapid accelerations of the body centre of mass is required. This study tests this prediction and examines its implemen- tation.

Will postural response strategy while leaning resemble a hip strategy as described for subjects standing across a narrow beam? Will changes in muscle activations, force patterns, or kinematics associated with change from an ankle to a more hip-like strategy appear discrete or gradual as subjects gradually approach their stability margins by leaning different amounts? Will subjects first maximize surface reactive torque and associated ankle muscle activation, and only then add shear forces associated with increased proximal muscle activation, or will they trigger, from the outset, a new movement strategy based on initial posture?

These questions must be addressed in order to better understand the neurophysiological basis of how the ner- vous system changes motor co-ordination based on functional demands. Are the changes in triggered, co-ordinative postural patterns consistent with well-established rules for modification of stretch reflexes by peripheral conditions or do they violate all known rules in order to accomplish functional goals under changing biomechanical constraints? For example, changes reported by Diener et ~11.28 in ankle muscle latencies and magnitudes in response to surface rotations while leaning are in the appropriate direction to be accounted for by either the biomechanical demands of the task or by local stretch reflex mechanisms’4-‘6. That is, when subjects leaned backwards, prelengthening and preactivating tibialis anterior and preshortening gastrocnemius prior to a toes up rotation, tibialis burst response to the rotation increased and its latency decreased and gastrocnemius response latency increased as would be expected from the dependence of stretch reflex thresholds on prelengthening or preactivating ankle musclesl”‘6, ‘9,

An advantage to examining the effects of prior leaning on responses to translations instead of rotations is that opposite effects would be predicted if changes are consistent with the functional biomechanical demands of the initial stance or with local stretch reflexes. If changes in

the postural response are due to the biomechanical demand of the situation, subjects would show increased latencies and decreased activation of prelengthened, preactivated ankle muscles associated with increased proximal muscle activation as subjects use more hip strategy. If changes in the muscle activation latencies and amplitudes are due to stretch- or load-dependent mechanisms resulting from prelengthening, preactivating or preshortening the distal muscles, we would expect shorter latencies and increased stretched-induced activation of prelengthened, preactivated muscles at the anklelkl6.29

Results from this study support the prediction that subjects change from an ankle to a hip strategy, similar to, but not identical to, a beam-balancing strategy, as they assume initial postures which bring them closer to their limits of stability. The observed changes in postural co-ordination can occur gradually as subjects use more and more proximal muscles and hip motions, as they approach their stability limits. Furthermore, results suggest that the CNS appears to trigger, from the outset, a new muscle activation pattern based on the initial posture. In ranges of initial stance well within stability limits, peripheral factors involving preactivation and prelengthening of ankle muscles can predict the observed changes in co-ordination of postural responses, but when subjects approach their limits of stability, only biomechanical constraints related to accomplishing the postural goal can explain the sometimes sudden changes in postural co-ordination.

Preliminary results have been presented previouslyjO.

Methods

Subjects and procedures

Six healthy normal subjects, between the ages of 21 and 32 years, stood, with arms crossed, on a hydraulically driven movable platform which translated forward or backward 6 cm in 240 ms (25 cm/s). Prior to the translation of the support surface, subjects were instructed to assume one of five initial anteroposterior (AP) stance positions by leaning about the ankles, keeping knee and hip angles erect: centre (comfortable stance), maximum forward, half-maximum forward, maximum backward and half-maximum backward. Maximum lean was determined after the subjects practised leaning as far forward and backward as possible without changing hip or knee position as observed by experimenter and later verified by kinematic analysis. AP stance position was monitored using a linear potentiometer attached via a rigid rod to a belt around the subjects’ hips. In order to assist subjects in reproducing the same five initial positions, this potentiometer signal was displayed on an oscilloscope provid- ing initial position feedback to the subject and the experimenter. The average maximum forward position, expressed as change in initial, centre potentiometer position, was 6.09 f 0.97” and maximum backward position was 4.76 f 0.44”. Half-forward position was 3.01 f 0.3” and half-backward position was 2.35 &

Horak and Moore: Effect of prior leaning on postural responses 205

0.12”. Subjects were instructed to return to centre or normal stance position between trials. Each subject performed 100 trials presented in blocks of 10 trials. For each block, subjects assumed one of the five initial positions; within a block there were five forward and five backward translations, randomly presented.

Recordings

Bipolar surface electrodes were used to examine the myoelectric activity of medial gastrocnemius (GAST) and tibialis anterior (TIB); biceps femoris (HAM) and rectus femoris (QUAD); and erector spinae (PARA) and rectus abdominis (ABD) of the right leg and trunk. The myoelectric signals were amplified and bandpass filtered at 70 and 1000 Hz. rectified and then low pass filtered (time constant 10 ms). Horizontal AP shear forces were measured from horizontal strain gauges mounted within the platform. The difference between anterior and posterior vertical forces measured from vertical strain gauges also mounted within the platform provided an estimate of torque generated primarily about the ankle joint, and will be referred to as ankle torque. Rectified electromyographic (EMG) activity, forces, AP stance position and platform position were collected at 500 Hz for I s, -including 100 ms baseline prior to platform displacement.

The kinematics of one subject were studied (sampling rate of 100 Hz) using a Watsmart motion analysis system. Infra-red light-emitting diodes were placed at approximate centres of joint rotation on the lateral aspect of the body such that it was possible to calculate ankle, knee and hip joint displacements which resulted from the horizontal translation.

Analysis

Onset latencies of EMG bursts were determined from individual trials as the first deviation of a burst over average background activity. Latencies were defined as the earliest time a sustained burst of EMG activity deviated from the pre-translation level of EMG activity and expressed with respect to the translation onset. Amplitudes of the EMG responses were determined by integrating, from a baseline of silent EMG, the first 75 ms of rectified EMG (IEMG) from onset of muscle activity response burst. (Over the 1 s of data collection, it was possible to identify a 100 ms period of silent EMG baseline, even for maximal lean trials.) The peak value of the active component of the AP shear force was measured and the average torque integral exerted from 150 ms to 500 ms following perturbation onset was calculated. Each of these variables were averaged across the last five trials of each stance position for each translation direction for each subject. IEMG were normalized by assigning the activated muscles in the centre stance position for anterior sway (gastrocnemius, hamstrings and paraspinals) and for posterior sway (tibialis, quadriceps and abdominals) a value of 1 and expressing values for other initial stance positions as a ratio. This EMG

normalization procedure allowed the combining of subjects’ data.

To examine the effect of initial stance position on distal muscle IEMG and onset latencies, a one-way analysis of variance (ANOVA) tested the effect of the five stance positions on gastrocnemius for anterior sway and tibialis anterior for posterior sway. To test the hypothesis that subjects switched from ankle to hip postural movement strategy, IEMG of the proximal muscles involved in the hip strategy for anterior sway (quadriceps and abdominals) and posterior sway (hamstrings and paraspinals) of each initial stance position were compared using a one-way ANOVA. Statistical analysis was also conducted on the force measures, integrated ankle torque and peak AP shear force, using a 2 by 5 (direction of perturbation by initial stance position) ANOVA with both factors repeated. A significance level of P < 0.01 was selected and post hoc analysis was performed using a Newman-Keuls procedure.

Results

EMG responses

A typical postural EMG response to an anterior sway perturbation (surface translated backward) with the subject standing in the normal centre position is shown in Figure la as the solid lines. This EMG response included activation of gastrocnemius, hamstrings and paraspinals in a distal to proximal order. When subjects leaned maximally forward, prelengthening the gastrocnemius, the antagonist thigh and trunk muscles (quadriceps and abdominals) also responded as shown with the dashed lines in Figure la. The solid bars indicate a 75 ms window of decreased gastrocnemius IEMG and increased paraspinal and hamstring IEMG response associated with maximum forward leaning. Note also the delayed activation of the gastrocnemius burst. To maintain the forward lean position, there was an increase in background tonic EMG of the prelengthened gastrocnemius and, in some subjects, increased tonic activity in hamstrings and paraspinals prior to the onset of the perturbation. This tonic activity in hamstrings and paraspinals was inhibited when the antagonist muscles (quadriceps and abdominals) were activated.

For posterior sway perturbations (surface translated forward), when subjects stood in the normal centred position, the ventral muscles, tibialis, quadriceps and abdominals, and often their antagonist trunk and thigh muscles (hamstrings and paraspinals), were activated in response to the 25 cm/s perturbations (solid line, Figure lb). When the subjects leaned maximally backward, prelengthening tibialis anterior, there was an increased activation of hamstrings and paraspinals, and an earlier but decreased activation of the distal prelengthened muscle tibialis in the time window shown by the black bars. To maintain this lean position, there was also an increase in tonic activity prior to the perturbation in tibialis and, in some cases, quadriceps and abdominals.

206 Gair & Posrure 1993; 1: No 4

a ANTERIOR SWAY b

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POSTERIOR SWAY

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-100 0 100 200 300 400

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Figure 1. EMG response pattern in response to anterior (a) and posterior (b) sway perturbations from a representative subject. The vertical line indicates the onset of the perturbation and the arrows under the stick figure indicate the direction of platform movement. The solid EMG lines represent the response during normal, centred stance position and the dashed EMG lines represent the response during maximal forward lean (a) and maximal backward lean (b). The heavy solid bars shows 75 ms window of GAS, HAM, ABD EMG for anterior sway and TI B, HAM, and PARA for posterior sway which were quantified in Figures 2 and 3. Each EMG response is an average of five trials.

The effects of initial stance position on the onset latency and activity level (IEMG) of the GAST response to anterior sway perturbations (Figure 2a) and of TIB responses to posterior sway perturbations are shown in Figure 2 with the statistical results of the ANOVA for each variable. A significant stance position effect was found for GAST latency. Consistent with prelengthening effects on stretch and load responses, the latency of GAST onset became shorter as GAST was gradually lengthened by initial stance in a maximum backward lean to a half-forward lean (Figure 2, top, right). How- ever, when subjects leaned maximally forward prior to an anterior sway perturbation, GAST latency was suddenly much prolonged, consistent with a switch to a hip strategy. Post hoc analysis indicated that the mean GAST response latency for maximum forward position (110 ms) was significantly greater than that for the centre (92 ms), half-forward (91 ms) and half-backward (94 ms) positions. Initial stance position did not have a statistically significant effect on GAST IEMG however (Figure 2, top, left).

A significant stance effect was found for both TIB latency and TIB IEMG for posterior sway (Figure 2, bottom). Like GAST, as initial TIB length was changed from a shortened length in maximum forward position to a longer length in half-backward position, TIB latency

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Figure 2. Bar graph of distal muscle mean activation level (I EMG) and onset latency of medial gastrocnemius response to anterior sway perturbations (top) and tibialis anterior to posterior sway perturbations (bottom) for each initial position. F-ratios and probability levels from analysis of variance are shown for each variable.

became progressively shorter (Figure 2, bottom, right). Also like GAST, when subjects leaned maximally in the same direction they were displaced (backward prior to posterior sway), TIB latency was suddenly prolonged. Post hoc analysis indicated that the TIB response latency for the half-back position (93 ms) was significantly different than for the other positions.

There was a greater effect of initial stance position on TIB activity level (IEMG) than for GAST (Figure 2, bottom, left). Consistent with a stretch or load effect, the maximum forward position (preshortened TIB) resulted in a significantly smaller TIB IEMG response (50% of neutral) than that observed for all other positions. How- ever, consistent with a change in movement strategy from ankle to hip, there was a decrease in TIB IEMG as subjects leaned backward prior to a backward sway displacement. Although this reduction in TIB IEMG to 82% of neutral was not statistically significant, all subjects showed this reduction in TIB IEMG.


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Figure 3. Bar graph of proximal muscle mean activation level (IEMG) of quadriceps and abdominals response to anterior sway perturbations (top) and hamstrings and paraspinals response to posterior sway perturbations (bottom) for each initial position. F-ratios and probability levels from analysis of variance are shown for each variable.

Changes in proximal muscle response amplitude with stance position reflected changes from an ankle to a hip postural movement strategy as subjects preleaned in the direction they were perturbed. Figure 3 shows the changes in the QUAD and ABD IEMG for anterior sway (Figure 3, top) and in HAM and PARA for posterior sway (Figure 3, bottom). There was a significant increase in the activity level of the ventral proximal muscles, QUAD and ABD as subjects leaned forward prior to anterior sway perturbations. QUAD and ABD IEMG were significantly greater in the maximum forward position compared with all other stance positions as indicated by the post hoc analysis. Similarly, as subjects leaned backward prior to a backward sway, there was a progressive increase in the activity level of the dorsal proximal muscles, HAM and QUAD. Post hoc analysis indicated that activation levels of both HAM and QUAD were significantly greater during both the maxi-

mal backward and half-backward stance positions compared with all other positions (Figure 3, bottom.) Changes in latencies of these proximal muscles could not be analysed statistically because they were often silent in the centre position.

Surface forces

When the maximal lean was in the same direction as the perturbation-induced AP sway, subjects changed from using predominantly ankle torque to using a combination of more horizontal shear force and less ankle torque to move the body centre of mass. Figure 4 shows the averaged AP shear and ankle torque traces of a representative subject for the centre (solid lines) and maximum forward (dashed lines, Figure 4, left) and maximum backward (dashed line, Figure 4, right) positions in response to anterior and posterior sway perturbations. Mean values for peak shear and integrated ankle torque for both sway directions are listed in Table 1. A significant direction by position interaction was found for integrated ankle torque (F4,16) = 7.379; P = 0.0014). Post hoc analysis indicated that, for anterior sway perturbations, average ankle plantarflexion torque was significantly less in the maximal forward lean position (4.878 Nm) than in all other positions (range 7.902-8.685 Nm). Similarly, for posterior sway perturbations, average ankle dorsiflexion torque was significantly less in the maximal backward lean position (4.293 Nm) than in the other four initial lean positions (range 6.355-7.981 Nm).

A significant direction by position interaction was also found for peak AP shear (F4,16) = 4,16), P = 0.0188). In contrast to torque, peak AP shear in response to anterior sway perturbations while in the maximium forward position (38.94 N) was significantly greater than in all other lean positions (range 17.01-24.86 N). The over- all effect of position was not significant for perturbations in the backward direction, although a significant increase in AP shear was found when subjects leaned maximally backward compared with the four other stance positions (34.50 compared with 25.52-26.91 N).

Kinematics

If the change from using primary ankle strategy to hip strategy occurs gradually as demanded by biomechanical constraints, a gradual increase in the amplitude of hip joint motions should be seen as subjects lean closer to their limits of stability. Averaged hip joint motions for the five initial stance positions in response to both forward and backward sway perturbations are shown in Figure 5 for a representative subject as shown in Figures 1 and 4. In the normal stance position and when leaning half-maximally and maximally away from the direction of imposed sway, normal hip joint angle was maintained at approximately 185” after the initial 2-4” hip perturbation. A large, active hip joint flexion (33”) occurred suddenly, only when the subject leaned maximally forward prior to a forward sway perturbation. In contrast, the amplitude of active hip joint extension increased

208 Gair & Posture 1993; 1: No 4

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Figure 4. Average (five trials) AP shear and torque during anterior (left) and posterior (right) sway perturbations from a representative subject whose EMGs were shown in Figure 1. Baseline offsets have been removed. Vertical line indicates the onset of perturbations. - Response for normal initial stance condition; - -- response for maximal forward lean in (a) and maximal backward lean in (b). The triangles indicate peak shear. The shaded area indicates the area integrated (350 ms) to measure average active torque. Positive AP shear indicates anterior direction. Positive ankle torque indicates dorsiflexion.

Table 1. Average ankle torque and AP shear for each initial position

Sway Maximum Half- Normal Half- Maximum direction forward forward stance backward backward

Ankle torque (Nm) Anterior 4.878” Posterior 6.355

AP shear (N) Anterior 38.94’ Posterior 26.91

l P < 0.01 in post hoc analysis.

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gradually (lo” and 32”) as the subject leaned progressively backward prior to a backward sway perturbation.

Discussion

must change to minimize muscle activations given the biomechanical constraints of a three-linked system attempting to quickly accelerate the body’s centre of mass while keeping the knees straight and heels and toes on the ground’-“.

Subjects used a different postural strategy when per- Some changes in postural responses with initial stance

turbed while leaning near their forward or backward posture, particularly when subjects remained well within limits of stability. These changes in postural strategy their limits of stability, could be explained by the well- were evident in the changed temporal organization and known effects of muscle length and preactivation on amplitude of the EMG bursts, the resulting forces on the stretch reflexesl”16. For example, consistent with changes support surface and the kinematics of the postural res- reported by Diener et aLZ8, TIB responses to a stretch ponse. These changes were not monotonically related to (induced here by a backward sway perturbation) gra- initial stance posture and cannot be explained by known dually increased in size and decreased in latency as it was rules of modification of stretch reflexes by peripheral lengthened from a preshortened position in forward lean conditions. These results support theoretical and compu- to a normal length in neutral stance. However, most of tational models that predict how postural co-ordination the observed changes cannot be predicted by such well-


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Figure 5. Hip displacement profile of five averaged trials to forward (top) and backward (bottom) sway perturbations for each initial stance condition for same representative subject as from Figures 1 and 4. Time is indicated in seconds with perturbation onset at 0.1 s and smaller hip angles indi- cating flexion. Prior leaning in the direction of a sway perturbation results in large hip flexion to recover for forward sway and hip extension to recover from backward sway.

known peripheral effects on local reflexes. For example, as subjects began to lean in the direction toward which they would be perturbed, preloading, preactivating and prelengthening ankle muscles resulted in a reduction, rather than an enhancement, of EMG and torque responses.

Although the tonic ankle torque and tonic ankle muscle EMG correlated with loading and stretching muscles due to leaning, the phasic torque and EMG burst responses were not significantly affected by prior leaning until subjects leaned maximally in the direction which they were perturbed. In this initial posture, phasic torque was suddenly reduced and changes in ankle muscle IEMG and latency reversed direction so magnitudes were reduced and latencies increased. These reductions in phasic torque would be necessary in order to keep the feet on the floor, given larger total torques as subjects leaned. Reduction in torque responses were accompa- nied by increases in hip-generated horizontal shear forces

in order to quickly move the centre of body mass before it exceeded the base of support2m3.

The co-ordinative postural responses pattern subjects used while leaning toward their limits of stability resem- bled the hip strategy used when subjects move the centre of mass quickly when standing across narrow beam96. Subjects showed larger hip motions, larger shear forces, and larger early proximal muscle activation both while leaning and while standing on beams. However, differences in the postural strategy used while leaning, from the hip strategy previously described for subjects on beams, are consistent with the biomechanical affordances of the two surfaces. While leaning on a normal surface, subjects continue to activate the stretched ankle muscle, although at reduced amplitudes and delayed latencies, unlike subjects on a beam who often eliminate ankle muscle activation or coactivate the ankle muscle@. In both instances of changing to use of more hip strategy to control equilibrium, the subjects trigger, from the outset, a new muscle and force pattern rather than adding a second pattern sequentially after a stereotyped initial response.

The changes in proximal muscle IEMG and changes in amount of hip angle displacement in response to backward sway suggested a continuous change in movement strategy with each position, whereas the changes in the responses to forward sway looked more discrete. This apparent difference in continuous versus discrete change in strategy for the two directions may be related to the steepness in the transition zone between the ankle and hip strategy. A surface translation brings a subject much closer to their stability limits when it evokes posterior sway compared with anterior sway due to biomechanical constraints of the limited amount of foot support behind the ankle joint. The half-backward lean position is closer to subjects’ limits of stability than the half-forward lean position. A gradual, continual blend of ankle and hip strategies could no doubt be observed if more initial stance positions were chosen.

Unfortunately, the effects of leaning prior to a postural perturbation have often been ignored in previous work on postural control. For example, some experimental paradigms for studying postural responses to surface tilt require subjects to assume a leaned position prior to trial onset-“.32, whereas others do not3). It is possible that some differences in findings between these groups may be accounted for by differences in initial stance position. Most studies have not required subjects to maintain a consistent initial stance position prior to a perturbation. This control of initial stance is important since subjects tend to unintentionally prelean in the direction of imposed sway they expect when initial stance position is not controlled34. Placing the centre of body mass even closer to limits of stable posture may not appear prudent unless one considers the biomechanical advantage that prestiffening and preactivating ankle muscles and trig- gering a hip strategy can have on increasing centre of mass acceleration’J. Initial stance position should also be considered in studies of postural control in patients with balance disorders since patients may assume leaning

210 Gait 81 Posture 1993; 1: No 4

positions either as an adaptive strategy or as a conse- of stretch reflex dynamics at the human ankle. Exp Brain

quence of altered biomechanical constraints33-37. Res 1986; 63: 49-59

In conclusion, the co-ordination of human postural responses changes as subjects lean about the ankles prior to a surface translation. These changes are consistent with computational models which suggest that biomechanical constraints and optimization <of muscle activation dictate a gradual change from an inverted pendulum-like ankle strategy to more hip strategy as subjects lean near their limits of stable posture.

17

18

19

Hammond PH. The influence of prior instruction to the subject on an apparently involuntary neuromuscular response. J Physiol (London) 1956; 122: 17-18 Evarts EV, Granit R. Relations of reflexes and intended movements. Prog Bruin Res 1976; 44: 1-14 Kearney RE, Hunter IW. System identification of human stretch reflex dynamics: tibialis anterior. Exp Bruin Res 1984; 56: 40-9

20

Acknowledgements 21

This research has been supported by a Postdoctoral Fellowship from the Natural Sciences and Engineering Council of Canada to SPM; and by grants CIDA NS01094 and NIA AGO6457 to FBH.

Diener HC, Horak FB, Nashner LM. Influence of stimulus parameters on human postural responses. J Neurophysioll988; 59: 1888-905 Massion J. Movement, posture and equilibrium: interaction and coordination. Prog Neurobioll992; 38: 3556

22 Hansen PD, Woollacott MH, Debu B. Postural responses to changing task conditions. Exp Brain Res 1988; 73: 627-36

23

References

Gurfinkle VS, Levik YS, Poppv KE, Smetanin BN, Shlikov VY. Body scheme in the control of postural activity. In: Gurfinkle VS, Yoffe, Massion J and Roll, eds. Stance and Motion: Facts and Theories. New York: Plenum Press, 1988: 185-193 Dunbar DC, Horak FB, Macpherson JM, Rushmer DS. Neural control of quadrupedal and bipedal stance: implications for the evolution of erect posture. Am J Phys Anthropoll986; 69: 93-105 Riccio GE, Stoffregen TA. Affordances as constraints on the control of stance. Human Mov Sci 1988; 7: 265-300 Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysioll986; 55: 1369-81 McCollum G, Horak FB, Nashner LM. Parsimony in neural calculations of postural movements. In: Bloedel J, Dichgans J and Precht W eds. Cerebellar Functions. Berlin: Springer Verlag, 1984; 52-66 Diener HC, Bootz F, Dichgans J, Bruzek W. Variability of postural ‘reflexes’ in humans. Exp Brain Res 1983; 52: 423-8

1

2

3

4

5

6

7

8

9

10

11

Nashner LM, McCollum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Bruin Sci 1985; 8: 132-72 Kuo A, Zajac FE. Human standing posture: multijoint movement strategies based on biomechanical constraints. Prog Brain Res 1993; 97: 349-58 Kuo A. An optimal control model for analysing human postural balance. IEEE Tram Biomed Eng, in press Gorden ME. Analysis of the biomechanics and muscular synergies of human standing. Unpublished PhD Dissertation, Stanford University, 1990 Nashner LM. Adapting reflexes controlling the human posture. Exp Brain Res 1976; 26: 59-72 Diener HC, Dichgans J, Bootz F. Functional plasticity of spinal and supraspinal reflexes in maintaining upright stance. Adv Otorhinoluryngof 1989; 30: 288-90 Moore SP, Rushmer DS, Windus SL, Nashner LM. Human automatic postural responses: responses to horizontal perturbations of stance in multiple directions, Exp Brain Res 1988; 73: 648-58 Gollhofer A, Horstmann GA, Berger W, Dietz V. Compensation of translational and rotational perturbations in human posture: stabilization of the centre of gravity. Neurosci Lett 1989; 105: 73-8 Macpherson JM, Horak FB, Dunbar DC. Stance dependence of automatic postural adjustments in humans. Exp Brain Res 1989; 78: 557-66 Horak FB, Nutt J, Nashner LM. Postural inflexibility in Parkinsonian subjects. J Neural Sci 1992; 111: 4658 Macpherson JM. How flexible are muscle synergies? In: Humphrey DR and Freund HJ, eds. Motor Control: Concepts and Issues. Chichester: John Wiley & Sons Ltd., 1991; 3347

12 Lacquaniti F, Borghese NA, Carrozzo M. Transient reversal of the stretch reflex in human arm muscles. J Neurophysioll991; 66: 939-54

13 Allum JHJ, Budingen HJ. The influence of initial foot inclination and head movements on counled stretch

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reflexes in ankle flexor and extensor muscles. Agressologie 1979: 20B: 143-4

14 Gottheb GL, Agawarl GC. Response to sudden torques about ankle in man: II. postmyotatic reactions. J NeurophysioZl980; 43: 86-101

15 Gottlieb GL, Agawarl GC. Response to sudden torques about ankle in man: III. suppression of stretch-evoked responses during phasic contraction. J NeurophysioZl980; 44: 233-46

16 Weiss PL, Kearney RE, Hunter IW. Position dependence

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Dietz V, Gollhofer A, Kleiber M, Trippel M. Regulation of bipedal stance: dependency on ‘load’ receptors. Exp Brain Res 1992; 89: 229-31 Moore SP, Horak FB, Nashner LM. Influence of initial stance position on human postural responses. Sot Neurosci Abs 1984; 56: 40-9 Allum JHJ, Pfaltz CR. Visual and vestibular contributions to pitch sway stabilization in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits. Exp Brian Res 1985; 58: 82-94 Do MC, Breniere Y, Bouisset S. Compensatory reaction in forward fall: are they initiated by stretch receptors? Electra Clin Neurophysiol 1988; 69: 448-52 Horak FB, Diener HC, Nashner LM. Influence of central set on human postural responses. J Neurophysiol 1989; 62: 841-53 Moore SP, Horak FB, Nashner LM. Influence of stimulus anticipation on human postural responses. Presented at the North American Society for the Psychology of Sport, June, 1986 Schieppati M, Nardone A. Free and supported stance in Parkinson’s disease: the effect of posture and ‘postural v ’ on leg muscle responses to perturbation, and its relation to the severity of the disease. Bruin 1991; 114: 1227-44 Horak FB, Shupert CL, Mirka A. Components of postural dyscontrol in the elderly: a review. Neurobiol Aging 1989; 10: 727-38 Black FO, Shupert CL, Horak FB, Nashner LM. Abnormal postural control associated with peripheral vestibular disorders. Prog Brain Res 1988; 76: 263-75

The effect of prior leaning on human postural responses

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